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Molecular Phylogenetics of the Bee-Eaters (Aves: Meropidae) Based on Nuclear and Mitochondrial DNA Sequence Data

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Molecular Phylogenetics of the Bee-Eaters (Aves: Meropidae) Based on Nuclear and Mitochondrial DNA Sequence Data Molecular Phylogenetics and Evolution 45 (2007) 23–32 www.elsevier.com/locate/ympev Molecular phylogenetics of the bee-eaters (Aves: Meropidae) based on nuclear and mitochondrial DNA sequence data Ben D. Marks a,*, Jason D. Weckstein b, Robert G. Moyle c a Department of Biological Sciences and Museum of Natural Science, Louisiana State University, 119 Foster Hall, Baton Rouge, LA 70808, USA b Zoology Department, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA c Department of Ornithology, American Museum of Natural History; Natural History Museum and Biodiversity Research Center, University of Kansas, KS, USA Received 19 October 2006; revised 27 June 2007; accepted 3 July 2007 Available online 18 July 2007 Abstract The bee-eaters (family Meropidae) comprise a group of brightly colored, but morphologically homogeneous, birds with a wide variety of life history characteristics. A phylogeny of bee-eaters was reconstructed using nuclear and mitochondrial DNA sequence data from 23 of the 25 named bee-eater species. Analysis of the combined data set provided a well-supported phylogenetic hypothesis for the family. Nyctiornis is the sister taxon to all other bee-eaters. Within the genus Merops, we recovered two well-supported clades that can be broadly separated into two groups along geographic and ecological lines, one clade with mostly African resident species and the other clade containing a mixture of African and Asian taxa that are mostly migratory species. The clade containing resident African species can be further split into two groups along ecological lines by habitat preference into lowland forest specialists and montane forest and forest edge species. Intraspecific sampling in several of the taxa revealed moderate to high (3.7–6.5%, ND2) levels of divergence in the resident taxa, whereas the lone migratory taxon showed negligible levels of intraspecific divergence. This robust molecular phylogeny provides the phylogenetic framework for future comparative tests of hypotheses about the evolution of plumage patterns, sociality, migration, and delayed breeding strategies. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Bee-eater; Meropidae; Systematics; Merops; Nyctiornis; Meropogon 1. Introduction and life history traits. Bee-eaters are distributed through- out the Old World, found in habitats ranging from the dri- The bee-eaters (family Meropidae) comprise a group of est of deserts to the wettest of rainforests. The family spans 25 species (Dickinson, 2003) of brightly colored, but mor- a spectrum ranging from sedentary tropical rainforest spe- phologically homogeneous, birds. As their common name cies to species that migrate between the temperate zone and suggests, bee-eaters feed primarily on bees and other the tropics for breeding and wintering. Some species of bee- Hymenoptera, which are usually plucked from the air in eaters nest solitarily, whereas others nest in large breeding gracefully aggressive foraging forays. Bee-eaters generally colonies. The young of some species delay breeding in their possess a conserved body plan with a long decurved bill, first year to serve as ‘‘helpers’’ at the nests of their parents long slender wings, a long tail (sometimes with elongated (Fry, 1972; Hegner et al., 1982). The remarkable level of central rectrices), and usually bold green or red base color- heterogeneity of behaviors (migratory, social, and breed- ation. The low level of morphological diversity in the fam- ing) among the bee-eaters is ideal for comparative study, ily is in stark contrast to their high diversity in ecological which requires a well-resolved phylogeny. However, until now there has been only a single formal analysis of bee- * Corresponding author. Fax: +1 225 578 3075. eater phylogenetic relationships (Burt, 2004) and no quan- E-mail address: [email protected] (B.D. Marks). titative assessment of support for relationships. 1055-7903/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2007.07.004 24 B.D. Marks et al. / Molecular Phylogenetics and Evolution 45 (2007) 23–32 Most authors recognize three genera in the family: Nyct- suggests that the phylogenetic signal in coloration charac- iornis, which includes two species of humid forest special- ters may be weak. ists inhabiting the rainforests of India and SE Asia, To test these proposed relationships among bee-eaters, Meropogon, a monotypic genus inhabiting forest edge we reconstructed a molecular phylogeny for the family and clearings in Sulawesi, and Merops, which includes 22 based on mitochondrial and nuclear DNA sequence data. species distributed across a variety of habitats throughout In the process, we resolve many phylogenetic and taxo- the Old World. Two of the most thorough investigations nomic uncertainties in the family and provide a phyloge- of the relationships among bee-eater species are those of netic framework for future comparative tests of von Boetticher (1951) and Fry (1969). Both studies were hypotheses about the evolution of plumage patterns, soci- based primarily on plumage (feather structure and color ality, migration and delayed breeding strategies. pattern) and morphometric features, although Fry (1969, 1984) also considered ecology and biogeography in produc- 2. Materials and methods ing his hypothesis of relationships. Although generic names applied in these revisions differed, the classifications were 2.1. Taxon and character sampling largely congruent, differing primarily in the placement of the African forest species (Merops muelleri, M. gularis, Ingroup sampling for our study (Table 1) included rep- and M. breweri). von Boetticher (1951) considered M. resentatives of 23 out of the 25 named species (Dickinson, breweri, a large and mostly solitary species, to be closely 2003), missing only Nycitornis athertoni and Merops revolii. related to the SE Asian N. amicta, N. athertoni,andMero- We also sampled two subspecies each for four of the species pogon forsteni and placed all four taxa in the genus Nyctior- (Table 1). Tissue samples were available for most taxa, but nis. The remaining African forest specialists (M. gularis for some taxa, only museum study-skin toepads or blood and M. muelleri) were placed in a separate genus Meropis- samples were available (Table 1). Outgoup taxa were cus. Fry (1969), using primarily biogeographic informa- drawn from other Coraciiform families; kingfishers, mot- tion, treated M. breweri as a member of Merops, but mots and todies. Genomic DNA was extracted from mus- later conceded that M. breweri may indeed be more closely cle tissue using the Qiagen DNeasy tissue kit following the related to Meropogon (Fry, 1984). Fry (1969, 1984) manufacturer’s protocol (Qiagen, Valencia, California). remained hesitant to group all of the lowland forest taxa Protocols for DNA extraction from museum skins gener- into Nyctiornis. These early hypotheses of relationships ally followed those for fresh tissues, with the addition of among bee-eater species, based on phenetic analyses of 10 ll of 1 M dithiothreitol solution. The protocols also morphological characters and life history data, were required special handling of samples and prevention of recently revisited by Burt (2004) in a comprehensive cladis- contamination, as described by Mundy et al. (1997). We tic analysis of 30 plumage-based and morphometric char- extracted, amplified, and sequenced all bee-eater tissue acters. The relationships inferred from Burt’s (2004) samples in the molecular labs at the LSU Museum of Nat- analysis were generally consistent with previous studies, ural Science and the Pritzker Laboratory at The Field but added M. hirundineus and M. boehmi to the list of taxa Museum, whereas the toepad samples were extracted, with enigmatic relationships. Burt (2004) found support for amplified, and sequenced in the Cullman Molecular Labo- a sister relationship between the African M. hirundineus ratory at the American Museum of Natural History. and the Australian M. ornatus, a relationship not sup- From the tissue samples we collected DNA sequence ported by either Fry (1969, 1984) or von Boetticher data from the entire second subunit of the mitochondrial (1951); both of whom place M. hirundineus in a superspe- nicotinamide adenine dinucleotide dehydrogenase gene cies consisting of other African bee-eaters (M. oreobates/ (ND2, 1041 bp) and two nuclear introns: the fifth intron pusillus/variegatus). In Burt’s (2004) four equally parsimo- of the nuclear b-fibrinogen gene (BFib5, 604 bp) and the nious trees, M. boehmi exhibited sister relationships with fifth intron of the transforming growth factor, b2 gene M. superciliosus/philippinus or M. viridis/leschenaulti, (TGFb2, 566 bp). For toepad samples we sequenced the whereas the earlier treatments placed M. boehmi close to entire second subunit of the ND2 gene (primers available the widespread M. orientalis (Fry, 1969) or the African upon request). We used primers L5215 (Hackett, 1996), M. albicollis (von Boetticher, 1951). The plumage charac- H6313, L5758, and H5766 (Johnson and Sorenson, 1998) ters used by Burt (2004) did not lend themselves to quanti- to amplify and sequence the ND2 gene, primers FIB5L tative analysis such as bootstrapping, and as a result there and FIB5H (Driskell and Christidis, 2004) to amplify and is no measure of support for the nodes depicted in his phy- sequence the Fib5 intron, and primers TGF5 and TGF6 logenetic hypothesis. Furthermore, plumage characters, (Primmer et al., 2002) to amplify and sequence the
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